Genetic Characterization of Two Novel Insect-Infecting Negative-Sense RNA Viruses Identified in a Leaf Beetle, Aulacophora indica
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Sample Preparation and RNA Extraction
2.2. Transcriptome and sRNA Sequencing
2.3. Host Insect Identification
2.4. Virus Discovery and Confirmation
2.5. Determination of Virus Full Length Genome and Transcript Abundance
2.6. Viral Genome Annotation and Phylogenetic Analysis
2.7. Small RNA Analysis
3. Results
3.1. Transcriptome Assembly and Virus Identification in A. indica
3.2. Genome Structure of Two Novel Negative-Sense RNA Viruses
3.3. Phylogenetic Analysis of Novel Viruses
3.4. Activation of the Antiviral RNA Interference Pathway in A. indica in Response to Novel Viruses
4. Discussion and Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Qi, Y.-H.; Ye, Z.-X.; Zhang, C.-X.; Chen, J.-P.; Li, J.-M. Diversity of RNA Viruses in Agricultural Insects. Comput. Struct. Biotechnol. J. 2023, 21, 4312–4321. [Google Scholar] [CrossRef]
- Bonning, B.C. The Insect Virome: Opportunities and Challenges. In Insect Molecular Virology: Advances and Emerging Trends; Caister Academic Press: Poole, UK, 2019; ISBN 978-1-912530-08-3. [Google Scholar]
- Käfer, S.; Paraskevopoulou, S.; Zirkel, F.; Wieseke, N.; Donath, A.; Petersen, M.; Jones, T.C.; Liu, S.; Zhou, X.; Middendorf, M.; et al. Re-Assessing the Diversity of Negative Strand RNA Viruses in Insects. PLoS Pathog. 2019, 15, e1008224. [Google Scholar] [CrossRef]
- Öhlund, P.; Lundén, H.; Blomström, A.-L. Insect-Specific Virus Evolution and Potential Effects on Vector Competence. Virus Genes 2019, 55, 127–137. [Google Scholar] [CrossRef]
- Nouri, S.; Matsumura, E.E.; Kuo, Y.-W.; Falk, B.W. Insect-Specific Viruses: From Discovery to Potential Translational Applications. Curr. Opin. Virol. 2018, 33, 33–41. [Google Scholar] [CrossRef] [PubMed]
- Wielkopolan, B.; Jakubowska, M.; Obrępalska-Stęplowska, A. Beetles as Plant Pathogen Vectors. Front. Plant Sci. 2021, 12, 748093. [Google Scholar] [CrossRef] [PubMed]
- Krell, R.K.; Pedigo, L.P.; Hill, J.H.; Rice, M.E. Bean Leaf Beetle (Coleoptera: Chrysomelidae) Management for Reduction of Bean Pod Mottle Virus. J. Econ. Entomol. 2004, 97, 192–202. [Google Scholar] [CrossRef] [PubMed]
- Smith, C.M.; Gedling, C.R.; Wiebe, K.F.; Cassone, B.J. A Sweet Story: Bean pod mottle virus Transmission Dynamics by Mexican Bean Beetles (Epilachna varivestis). Genome Biol. Evol. 2017, 9, 714–725. [Google Scholar] [CrossRef]
- Gergerich, R.C. Mechanism of Virus Transmission by Leaf-Feeding Beetles. In Virus-Insect-Plant Interactions; Academic Press: Cambridge, MA, USA, 2001; pp. 133–142. [Google Scholar]
- Bradshaw, J.D.; Rice, M.E.; Hill, J.H. Evaluation of Management Strategies for Bean Leaf Beetles (Coleoptera: Chrysomelidae) and Bean Pod Mottle Virus (Comoviridae) in Soybean. J. Econ. Entomol. 2008, 101, 1211–1227. [Google Scholar] [CrossRef]
- Lee, C.-F.; Beenen, R. Revision of the Genus Aulacophora from Taiwan (Coleoptera: Chrysomelidae: Galerucinae). Zootaxa 2015, 3949, 151–190. [Google Scholar] [CrossRef]
- Jiang, W.; Yu, X.; Zhang, H.; Wang, Y.; Tian, X. The Complete Mitochondrial Genome Sequence of Aulacophora Indica. Mitochondrial DNA Part B 2020, 5, 184–185. [Google Scholar] [CrossRef]
- Liu, S.; Sappington, T.W.; Coates, B.S.; Bonning, B.C. Nudivirus Sequences Identified from the Southern and Western Corn Rootworms (Coleoptera: Chrysomelidae). Viruses 2021, 13, 269. [Google Scholar] [CrossRef] [PubMed]
- Ye, Z.-X.; Li, Y.-H.; Chen, J.-P.; Zhang, C.-X.; Li, J.-M. Complete Genome Analysis of a Novel Iflavirus from a Leaf Beetle, Aulacophora Lewisii. Arch. Virol. 2021, 166, 309–312. [Google Scholar] [CrossRef] [PubMed]
- Huang, H.-J.; Ye, Z.-X.; Wang, X.; Yan, X.-T.; Zhang, Y.; He, Y.-J.; Qi, Y.-H.; Zhang, X.-D.; Zhuo, J.-C.; Lu, G.; et al. Diversity and Infectivity of the RNA Virome among Different Cryptic Species of an Agriculturally Important Insect Vector: Whitefly Bemisia Tabaci. NPJ Biofilms Microbiomes 2021, 7, 43. [Google Scholar] [CrossRef]
- Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; et al. Full-Length Transcriptome Assembly from RNA-Seq Data without a Reference Genome. Nat. Biotechnol. 2011, 29, 644–652. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Andika, I.B.; Zhou, Y.; Shen, J.; Sun, Z.; Wang, X.; Sun, L.; Chen, J. Unusual Characteristics of Dicistrovirus-Derived Small RNAs in the Small Brown Planthopper, Laodelphax striatellus. J. Gen. Virol. 2014, 95, 712–718. [Google Scholar] [CrossRef]
- Buchfink, B.; Xie, C.; Huson, D.H. Fast and Sensitive Protein Alignment Using DIAMOND. Nat. Methods 2015, 12, 59–60. [Google Scholar] [CrossRef] [PubMed]
- Langmead, B.; Salzberg, S.L. Fast Gapped-Read Alignment with Bowtie 2. Nat. Methods 2012, 9, 357–359. [Google Scholar] [CrossRef]
- Thorvaldsdottir, H.; Robinson, J.T.; Mesirov, J.P. Integrative Genomics Viewer (IGV): High-Performance Genomics Data Visualization and Exploration. Brief. Bioinform. 2013, 14, 178–192. [Google Scholar] [CrossRef]
- Chen, C.; Wu, Y.; Li, J.; Wang, X.; Zeng, Z.; Xu, J.; Liu, Y.; Feng, J.; Chen, H.; He, Y.; et al. TBtools-II: A “One for All, All for One” Bioinformatics Platform for Biological Big-Data Mining. Mol. Plant 2023, 16, 1733–1742. [Google Scholar] [CrossRef]
- Xiang, C.-Y.; Gao, F.; Jakovlić, I.; Lei, H.-P.; Hu, Y.; Zhang, H.; Zou, H.; Wang, G.-T.; Zhang, D. Using PhyloSuite for Molecular Phylogeny and Tree-Based Analyses. iMeta 2023, 2, e87. [Google Scholar] [CrossRef]
- Katoh, K.; Standley, D.M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [PubMed]
- Capella-Gutiérrez, S.; Silla-Martínez, J.M.; Gabaldón, T. trimAl: A Tool for Automated Alignment Trimming in Large-Scale Phylogenetic Analyses. Bioinformatics 2009, 25, 1972–1973. [Google Scholar] [CrossRef]
- Nguyen, L.-T.; Schmidt, H.A.; Von Haeseler, A.; Minh, B.Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef] [PubMed]
- Clewley, J.P.; Arnold, C. MEGALIGN. In Sequence Data Analysis Guidebook; Swindell, S.R., Ed.; Springer: Totowa, NJ, USA, 1997; pp. 119–129. ISBN 978-1-59259-556-3. [Google Scholar]
- Nakashima, N.; Kawahara, N.; Omura, T.; Noda, H. Characterization of a Novel Satellite Virus and a Strain of Himetobi P Virus (Dicistroviridae) from the Brown Planthopper, Nilaparvata lugens. J. Invertebr. Pathol. 2006, 91, 53–56. [Google Scholar] [CrossRef] [PubMed]
- Ren, P.-P.; Ye, Z.-X.; Wang, S.-N.; Li, J.-M.; Chen, J.-P.; Zhang, C.-X.; Lu, J.-B. Complete Genome Analysis of a Novel Chuvirus from a Southern Green Stink Bug (Nezara viridula). Arch. Virol. 2022, 167, 2423–2427. [Google Scholar] [CrossRef]
- Kuhn, J.H.; Dheilly, N.M.; Junglen, S.; Paraskevopoulou, S.; Shi, M.; Di Paola, N. ICTV Virus Taxonomy Profile: Jingchuvirales 2023: This Article Is Part of the ICTV Virus Taxonomy Profiles Collection. J. Gen. Virol. 2023, 104, 001924. [Google Scholar] [CrossRef]
- Ding, S.-W. RNA-Based Antiviral Immunity. Nat. Rev. Immunol. 2010, 10, 632–644. [Google Scholar] [CrossRef]
- Bonning, B.C.; Saleh, M.-C. The Interplay Between Viruses and RNAi Pathways in Insects. Annu. Rev. Entomol. 2021, 66, 61–79. [Google Scholar] [CrossRef]
- Gammon, D.B.; Mello, C.C. RNA Interference-Mediated Antiviral Defense in Insects. Curr. Opin. Insect. Sci. 2015, 8, 111–120. [Google Scholar] [CrossRef]
- Aguiar, E.R.G.R.; Olmo, R.P.; Marques, J.T. Virus-derived Small RNAs: Molecular Footprints of Host–Pathogen Interactions. Wiley Interdiscip. Rev. RNA 2016, 7, 824–837. [Google Scholar] [CrossRef]
- Da Silva, L.A.; Basso, M.F.; Ribeiro, B.M. A Novel Picorna-like Virus Identified in the Cotton Boll Weevil Anthonomus Grandis (Coleoptera: Curculionidae). Arch. Virol. 2023, 168, 29. [Google Scholar] [CrossRef]
- Li, C.-X.; Shi, M.; Tian, J.-H.; Lin, X.-D.; Kang, Y.-J.; Chen, L.-J.; Qin, X.-C.; Xu, J.; Holmes, E.C.; Zhang, Y.-Z. Unprecedented Genomic Diversity of RNA Viruses in Arthropods Reveals the Ancestry of Negative-Sense RNA Viruses. eLife 2015, 4, e05378. [Google Scholar] [CrossRef] [PubMed]
- Jones, K.E.; Patel, N.G.; Levy, M.A.; Storeygard, A.; Balk, D.; Gittleman, J.L.; Daszak, P. Global Trends in Emerging Infectious Diseases. Nature 2008, 451, 990–993. [Google Scholar] [CrossRef]
- Kuhn, J.H.; Abe, J.; Adkins, S.; Alkhovsky, S.V.; Avšič-Županc, T.; Ayllón, M.A.; Bahl, J.; Balkema-Buschmann, A.; Ballinger, M.J.; Kumar Baranwal, V.; et al. Annual (2023) Taxonomic Update of RNA-Directed RNA Polymerase-Encoding Negative-Sense RNA Viruses (Realm Riboviria: Kingdom Orthornavirae: Phylum Negarnaviricota). J. Gen. Virol. 2023, 104, 001864. [Google Scholar] [CrossRef]
- ICTV Report Chapters. Available online: https://ictv.global/report/chapter/nyamiviridae/nyamiviridae/formivirus (accessed on 24 June 2024).
- Dietzgen, R.G.; Firth, A.E.; Jiāng, D.; Junglen, S.; Kondo, H.; Kuhn, J.H.; Paraskevopoulou, S.; Vasilakis, N. ICTV Report Consortium ICTV Virus Taxonomy Profile: Nyamiviridae 2021. J. Gen. Virol. 2021, 102, 001681. [Google Scholar] [CrossRef]
- Kuhn, J.H.; Bekal, S.; Caì, Y.; Clawson, A.N.; Domier, L.L.; Herrel, M.; Jahrling, P.B.; Kondo, H.; Lambert, K.N.; Mihindukulasuriya, K.A.; et al. Nyamiviridae: Proposal for a New Family in the Order Mononegavirales. Arch. Virol. 2013, 158, 2209–2226. [Google Scholar] [CrossRef] [PubMed]
- Mihindukulasuriya, K.A.; Nguyen, N.L.; Wu, G.; Huang, H.V.; Travassos Da Rosa, A.P.A.; Popov, V.L.; Tesh, R.B.; Wang, D. Nyamanini and Midway Viruses Define a Novel Taxon of RNA Viruses in the Order Mononegavirales. J. Virol. 2009, 83, 5109–5116. [Google Scholar] [CrossRef]
- Bekal, S.; Domier, L.L.; Niblack, T.L.; Lambert, K.N. Discovery and Initial Analysis of Novel Viral Genomes in the Soybean Cyst Nematode. J. Gen. Virol. 2011, 92, 1870–1879. [Google Scholar] [CrossRef]
- Dhaygude, K.; Johansson, H.; Kulmuni, J.; Sundström, L. Genome Organization and Molecular Characterization of the Three Formica Exsecta Viruses—FeV1, FeV2 and FeV4. PeerJ 2019, 6, e6216. [Google Scholar] [CrossRef]
- Di Paola, N.; Dheilly, N.M.; Junglen, S.; Paraskevopoulou, S.; Postler, T.S.; Shi, M.; Kuhn, J.H. Jingchuvirales: A New Taxonomical Framework for a Rapidly Expanding Order of Unusual Monjiviricete Viruses Broadly Distributed among Arthropod Subphyla. Appl. Environ. Microbiol. 2022, 88, e01954-21. [Google Scholar] [CrossRef]
- Shi, M.; Lin, X.-D.; Tian, J.-H.; Chen, L.-J.; Chen, X.; Li, C.-X.; Qin, X.-C.; Li, J.; Cao, J.-P.; Eden, J.-S.; et al. Redefining the Invertebrate RNA Virosphere. Nature 2016, 540, 539–543. [Google Scholar] [CrossRef]
- He, W.-T.; Hou, X.; Zhao, J.; Sun, J.; He, H.; Si, W.; Wang, J.; Jiang, Z.; Yan, Z.; Xing, G.; et al. Virome Characterization of Game Animals in China Reveals a Spectrum of Emerging Pathogens. Cell 2022, 185, 1117–1129. [Google Scholar] [CrossRef] [PubMed]
- Geoghegan, J.L.; Di Giallonardo, F.; Wille, M.; Ortiz-Baez, A.S.; Costa, V.A.; Ghaly, T.; Mifsud, J.C.O.; Turnbull, O.M.H.; Bellwood, D.R.; Williamson, J.E.; et al. Virome Composition in Marine Fish Revealed by Meta-Transcriptomics. Virus Evol. 2021, 7, veab005. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.-M.; Sadiq, S.; Tian, J.-H.; Chen, X.; Lin, X.-D.; Shen, J.-J.; Chen, H.; Hao, Z.-Y.; Wille, M.; Zhou, Z.-C.; et al. RNA Viromes from Terrestrial Sites across China Expand Environmental Viral Diversity. Nat. Microbiol. 2022, 7, 1312–1323. [Google Scholar] [CrossRef]
- Harvey, E.; Holmes, E.C. Diversity and Evolution of the Animal Virome. Nat. Rev. Microbiol. 2022, 20, 321–334. [Google Scholar] [CrossRef]
- Obbard, D.J.; Shi, M.; Roberts, K.E.; Longdon, B.; Dennis, A.B. A New Lineage of Segmented RNA Viruses Infecting Animals. Virus Evol. 2020, 6, vez061. [Google Scholar] [CrossRef] [PubMed]
- Aguiar, E.R.G.R.; Olmo, R.P.; Paro, S.; Ferreira, F.V.; de Faria, I.J.d.S.; Todjro, Y.M.H.; Lobo, F.P.; Kroon, E.G.; Meignin, C.; Gatherer, D.; et al. Sequence-Independent Characterization of Viruses Based on the Pattern of Viral Small RNAs Produced by the Host. Nucleic Acids Res. 2015, 43, 6191–6206. [Google Scholar] [CrossRef]
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Chen, M.-N.; Ye, Z.-X.; Feng, K.-H.; Yuan, J.-N.; Chen, J.-P.; Zhang, C.-X.; Li, J.-M.; Mao, Q.-Z. Genetic Characterization of Two Novel Insect-Infecting Negative-Sense RNA Viruses Identified in a Leaf Beetle, Aulacophora indica. Insects 2024, 15, 615. https://doi.org/10.3390/insects15080615
Chen M-N, Ye Z-X, Feng K-H, Yuan J-N, Chen J-P, Zhang C-X, Li J-M, Mao Q-Z. Genetic Characterization of Two Novel Insect-Infecting Negative-Sense RNA Viruses Identified in a Leaf Beetle, Aulacophora indica. Insects. 2024; 15(8):615. https://doi.org/10.3390/insects15080615
Chicago/Turabian StyleChen, Meng-Nan, Zhuang-Xin Ye, Ke-Hui Feng, Jing-Na Yuan, Jian-Ping Chen, Chuan-Xi Zhang, Jun-Min Li, and Qian-Zhuo Mao. 2024. "Genetic Characterization of Two Novel Insect-Infecting Negative-Sense RNA Viruses Identified in a Leaf Beetle, Aulacophora indica" Insects 15, no. 8: 615. https://doi.org/10.3390/insects15080615